Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

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Abstract
The medial bed nucleus of the stria terminalis (BSTm) influences both social approach and social aversion, suggesting that this structure may play an important role in generating motivational and behavioral differences between gregarious and asocial species. However, no specific neurons have been identified within the BSTm that influence species-typical levels of sociality or that mediate approach and avoidance. Using five songbird species that differ selectively in their species-typical group sizes, we now demonstrate that vasotocin-immunoreactive (VT-ir) neurons of the BSTm exhibit very different immediate early gene responses to same-sex stimuli in gregarious and asocial species. Exposure to a same-sex conspecific increases VT-Fos colocalization in gregarious species while decreasing colocalization in relatively asocial species. We additionally demonstrate that these neurons are selectively activated by social stimuli that normally elicit affiliation (positively valenced social stimuli) but not by stimuli that elicit aversion (negatively valenced social stimuli). Constitutive Fos activity of the VT-ir neurons is also significantly greater in the gregarious species, and the two most social species express significantly more VT-ir neurons. These findings demonstrate that the properties of valence-sensitive neurons evolve in relation to sociality and indicate that gregarious species accentuate positive stimulus properties during social interactions.